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Journal of Human Evolution 76 (2014) 154e164

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Journal of Human Evolution

journal homepage: www.elsevier .com/locate/ jhevol

Out of Africa, but how and when? The case of hamadryas baboons(Papio hamadryas)

Gisela H. Kopp a, *, Christian Roos b, Thomas M. Butynski c, d, 1, Derek E. Wildman e,Abdulaziz N. Alagaili f, g, Linn F. Groeneveld h, Dietmar Zinner a

a Cognitive Ethology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 G€ottingen, Germanyb Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4,37077 G€ottingen, Germanyc King Khalid Wildlife Research Centre, Saudi Wildlife Authority, P.O. Box 61681, Riyadh 11575, Saudi Arabiad Conservation Programs, Zoological Society of London, Regent's Park, London NW1 4RY, United Kingdome Center for Molecular Medicine and Genetics, Wayne State University School of Medicine, 540 E. Canfield Ave. 3240 Scott Hall, Detroit, MI 48220, USAf KSU Mammals Research Chair, Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabiag Saudi Wildlife Authority, P.O. Box 61681, Riyadh 11575, Saudi Arabiah NordGen e Nordic Genetic Resource Center, Ås, Norway

a r t i c l e i n f o

Article history:Received 22 April 2014Accepted 7 August 2014Available online 23 September 2014

Keywords:HVRIArabiaPleistoceneDivergence time estimatesPopulation structurePrimate

* Corresponding author.E-mail addresses: gkopp@dpz.eu (G.H. Kopp), croos

aol.com (T.M. Butynski), dwildman@med.wayne.edu (edu.sa (A.N. Alagaili), linn.groeneveld@nordgen.orggwdg.de (D. Zinner).

1 Present affiliation: Lolldaiga Hills Research ProgEastern Africa, P.O. Box 149, Nanyuki 10400, Kenya.

http://dx.doi.org/10.1016/j.jhevol.2014.08.0030047-2484/© 2014 The Authors. Published by Elsevier

a b s t r a c t

Many species of Arabian mammals are considered to be of Afrotropical origin and for most of them theRed Sea has constituted an obstacle for dispersal since the MioceneePliocene transition. There are twopossible routes, the ‘northern’ and the ‘southern’, for terrestrial mammals (including humans) to movebetween Africa and Arabia. The ‘northern route’, crossing the Sinai Peninsula, is confirmed for severaltaxa by an extensive fossil record, especially from northern Egypt and the Levant, whereas the ‘southernroute’, across the Bab-el-Mandab Strait, which links the Red Sea with the Gulf of Aden, is morecontroversial, although post-Pliocene terrestrial crossings of the Red Sea might have been possibleduring glacial maxima when sea levels were low.

Hamadryas baboons (Papio hamadryas) are the only baboon taxon to disperse out of Africa and stillinhabit Arabia. In this study, we investigate the origin of Arabian hamadryas baboons using mitochon-drial sequence data from 294 samples collected in Arabia and Northeast Africa. Through the analysis ofthe geographic distribution of genetic diversity, the timing of population expansions, and divergencetime estimates combined with palaeoecological data, we test: (i) if Arabian and African hamadryas ba-boons are genetically distinct; (ii) if Arabian baboons exhibit population substructure; and (iii) when, andvia which route, baboons colonized Arabia.

Our results suggest that hamadryas baboons colonized Arabia during the Late Pleistocene (130e12 kya[thousands of years ago]) and also moved back to Africa. We reject the hypothesis that hamadryas ba-boons were introduced to Arabia by humans, because the initial colonization considerably predates theearliest records of human seafaring in this region. Our results strongly suggest that the ‘southern route’from Africa to Arabia could have been used by hamadryas baboons during the same time period asproposed for modern humans.© 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND

license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

@dpz.eu (C. Roos), tbutynski@D.E. Wildman), aalagaili@ksu.(L.F. Groeneveld), dzinner@

ramme, Sustainability Centre

Ltd. This is an open access article u

Introduction

When modern humans (Homo sapiens) dispersed out of Africais a central question in the study of human evolution. Recentlydiscovered archaeological evidence in Jebel Faya, United ArabEmirates, points to the presence of modern humans in Arabia by ca.125 thousand years ago (kya) (Armitage et al., 2011). That studystresses the Bab-el-Mandab Strait in the southern Red Sea as apossible immigration route during glacial maxima, when sea levels

nder the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164 155

were low, as an alternative to a northern route via the SinaiPeninsula (Beyin, 2006, 2011). Humans are not the only mammalthat evolved in Africa and colonized Arabia. Many species ofArabian mammals are considered to be of Afrotropical origin(Delany, 1989), with 62 species in nine orders known to occur onboth sides of the Red Sea (Harrison and Bates, 1991; Yalden et al.,1996). These taxa colonized Arabia at different times. For most ofthem the Red Sea has constituted an obstacle for dispersal since theMioceneePliocene transition 5.3 million years ago (mya)(Fernandes et al., 2006; Bailey et al., 2007; Bailey, 2009). There aretwo routes, the ‘northern’ and the ‘southern’, that would haveenabled terrestrial mammals to move between Africa and Arabia(Beyin, 2006, 2011; Bailey, 2009) (Fig. 1). The ‘northern route’,crossing the Sinai Peninsula, is confirmed for several taxa by anextensive fossil record, especially from northern Egypt and theLevant (Tchernov, 1992; Cavalli-Sforza et al., 1993; Lahr and Foley,1994). Immigrations via this route presumably occurred duringseveral ‘Green Sahara Periods’ when humid conditions openeddispersal corridors across the eastern Sahara for savannah species(Blome et al., 2012; Drake et al., 2013; Larrasoa~na et al., 2013). The‘southern route’, across the Bab-el-Mandab Strait, which links theRed Seawith the Gulf of Aden, is more controversial, although post-Pliocene (2.5 mya) terrestrial crossings of the Red Sea might havebeen possible during glacial maxima when sea levels were low(Bailey et al., 2007). There is, however, disagreement as to whetherthe palaeoceanographic and palaeoecological data are compatiblewith the scenario of land bridges (Rohling, 1994; deMenocal, 1995;Rohling et al., 1998, 2009; Siddall et al., 2003; Fernandes et al.,2006).

Baboons (Papio spp.) have been proposed as an analogousmodel for human evolution as they evolved during the same periodand in the same habitats (Jolly, 1970, 2001; Strum and Mitchell,

Figure 1. Geographic range and hypothetical immigration routes of hamadryas ba-boons from Africa into Arabia. Dashed lines indicate the approximate borders of thegeographic range of hamadryas baboon in Africa and Arabia (after Yalden et al., 1977,1996; Harrison and Bates, 1991). Thick arrows indicate the southern and northerndispersal routes.

1987; Rodseth et al., 1991; Elton, 2006). At present, five or sixspecies of baboons are usually recognized, although their taxo-nomic status is still debated: chacma (Papio ursinus), Kinda (Papiokindae), yellow (Papio cynocephalus), olive (Papio anubis), hama-dryas (Papio hamadryas), and Guinea baboon (Papio papio) (Jolly,1993, 2013; Kingdon, 1997; Szmulewicz et al., 1999; Groves,2001; Frost et al., 2003; Grubb et al., 2003; Zinner et al., 2009;Anandam et al., 2013; Butynski et al., 2013). The fossil record andmitochondrial sequence data both suggest that modern Papiooriginated in southern Africa ca. 2.5 mya, from where theydispersed to the north and west (Benefit, 1999; Newman et al.,2004; Zinner et al., 2011, 2013). The current distribution of Papioincludes much of sub-Saharan Africa, excluding most of the centraland West African rain forests. The hamadryas baboon is the onlybaboon found outside of Africa and one of the few primate speciesexhibiting female-biased dispersal (Hapke et al., 2001; Hammondet al., 2006; Kopp et al., 2014). At present, this species inhabitsEthiopia, Eritrea, Somalia, Djibouti and possibly Sudan, and south-western Arabia along the Red Sea from Yemen to south-westernSaudi Arabia (Anandam et al., 2013; Swedell, 2013) (Fig. 1). Cra-nial and dental remains of Papio sp. from the Middle Pleistocene(800e200 kya) recovered at Asbole, Ethiopia, show strong affinitiesto extant P. hamadryas (Alemseged and Geraads, 2000), indicating along presence of hamadryas baboons on the African side of the RedSea.

The hamadryas baboons of Arabia were thought to be smallerthan those in Africa and, as such, referred to as Papio arabicus(Thomas, 1900) or P. hamadryas arabicus (Ellermann and Morrison-Scott, 1951; Harrison, 1964; Corbet, 1978; Harrison and Bates, 1991).Kummer et al. (1981) found, however, that hamadryas baboons onboth sides of the Red Sea are morphologically and behaviourallysimilar. Groves (2001, 2005) also found no significant differencesbetween African and Arabian representatives of this species and, assuch, considers hamadryas baboons as monotypic.

Three hypotheses have been put forth to explain the presence ofhamadryas baboons in Arabia (Kummer, 1995):

(i) Hamadryas baboons in Arabia are remnants of a pastcontinuous distribution around the Red Sea (northern route;Fig. 1). To our knowledge, however, no Papio fossils or sub-fossils have been discovered in the Levant, in northern Egypt,or in northwestern Arabia. Dispersal events could have beenfavoured during Green Sahara Periods, e.g., in Marine Iso-topic Stage (MIS) 5 (130e71 kya; Blome et al., 2012; Drakeet al., 2013; Larrasoa~na et al., 2013).

(ii) Hamadryas baboons immigrated to Arabia across thesouthern Red Sea (southern route; Fig. 1), e.g., via a tempo-rary land bridge, during periods of sea level lowstand of theRed Sea (MIS 12: ca. 440 kya; MIS 10: ca. 340 kya; MIS 6: ca.130 kya; MIS 4: ca. 65 kya; MIS 2: ca. 20 kya; Rohling, 1994;Rohling et al., 1998, 2009).

(iii) Hamadryas baboons were introduced into Arabia by humans(Thomas, 1900; Kummer et al., 1981). Ancient Egyptians areknown to have translocated baboons. For example, there aredrawings from the Eighteenth Dynasty (1540e1304 Beforethe Common Era [B.C.E.]) in which boats from Punt (which isprobably Eritrea) brought hamadryas baboons to Egypt(Kummer, 1995; Moritz et al., 2010). It is conceivable thatthese ships reached Arabia (Phillips,1997). Moreover, there isevidence for trade between Northeast Africa and Arabiaduring earlier times, e.g., in the Predynastic Period(5000e3100 B.C.E.; Ward, 2006; Boivin and Fuller, 2009;Boivin et al., 2009) and the Bronze Age (c. 3500e1200B.C.E.; Boivin and Fuller, 2009; Boivin et al., 2009), which hadthe potential for the translocation of baboons.

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164156

To date, there are three population genetic studies that focus onthe origin of Arabian hamadryas baboons. The first study investi-gated the phylogeography of Arabian hamadryas baboons (Winneyet al., 2004) using 168 base pair (bp) sequences of the mitochon-drial hypervariable region I (HVRI) of 107 baboon samples from foursites in Saudi Arabia plus sequences published by Hapke et al.(2001) from 10 sites in Eritrea. Of the three clades recovered,Clade 1 is found only in Arabia, Clade 2 is mainly African but alsopresent in the southernmost sampling location in Arabia, and Clade3 is found only in Africa. Divergence dates were calculated based onthe human/chimpanzee split and on the transition/transversionratio, leading to estimates of the most recent common ancestor ofall clades at 443e316 kya. Divergence dates within Clades 1 and 2were estimated at 119e85 kya and 219e156 kya, respectively.Winney et al. (2004) concluded that, assuming an African origin ofhamadryas baboons and a later colonization of Arabia, the diver-gence time estimates point to immigration events before humanscould have played a role. The Winney et al. (2004) study has somelimitations, namely (i) a sampling regime that does not includeYemen, Ethiopia or any region close to Bab-el-Mandab, (ii) roughdivergence estimates without confidence intervals, and (iii) anal-ysis based on only a very short, highly variable, fragment of onemitochondrial DNA (mtDNA) locus.

A second study, by Wildman (2000) and Wildman et al. (2004),analysed 47 baboon samples, including hamadryas baboons fromfive sites in Yemen, three sites in Saudi Arabia, and one site inEthiopia. Based on a different and less variable mitochondrialmarker (Brown Region, 896 bp; Brown et al., 1982) than theWinneyet al. (2004) study, they found three clades: the exclusively ArabianClade IIA (part of Winney's Clade 2), Clade IIB, which includeshamadryas baboons of Arabia and Ethiopia with a purely Arabiansubclade (Winney's Clade 1), and Clade IIC, which includes Africanhamadryas and olive baboons (Winney's Clade 3). Due to the tri-chotomy of Clade II, this study did not draw a conclusion on wherehamadryas baboons evolved, but argued that an African origin ismost parsimonious. Calibrated with a palaeontologically docu-mented 4 mya Theropithecus-Papio split (Delson, 1993; Goodmanet al., 1998; Gundling and Hill, 2000), they dated the colonizationof Arabia close to the origin of hamadryas baboons (ca. 400 kya) andexcluded gene flow between Africa and Arabia after ca. 35 kya. Theythereby also rejected the hypothesis of human introduction.Wildman (2000) and Wildman et al. (2004) suggested that hama-dryas baboons colonized Arabia multiple times via the southernroute with a first dispersal event in the Middle Pleistocene (after400 kya).

A third study, by Fernandes (2009), reviewed the data on theorigin of Arabian baboons (Wildman et al., 2004; Winney et al.,2004) and applied two Bayesian coalescent approaches to resolvethe discordance between the estimated colonization times of thetwo earlier studies. He concluded that hamadryas baboons colo-nized Arabia twice, and suggested two northern expansions intoArabia during interglacial periods [MIS 9e (ca. 330 kya) or MIS 7c(ca. 220 kya), and the second half of MIS 5e (120e110 kya) or theend of MIS 5a (ca. 80 kya)]. However, the estimates provided by thetwo approaches differed considerably and, in our opinion, the verylarge confidence intervals make it impossible to draw conclusionsabout the most probable immigration route.

In our study, we investigate the origin of Arabian hamadryasbaboons. We use mitochondrial sequence data from 294 baboonsamples collected in Arabia and in Northeast Africa. These enableus to more accurately determine the distribution of the clades andto assess whether the pure Arabian clade found in the earlierstudies is, in fact, only present in Arabia. We sequenced threemtDNAmarkers, summing up to a total length of 2373 bp, to obtaina better resolution of divergence time estimates. Furthermore, we

conducted more sophisticated Bayesian time divergence estimatesincluding confidence intervals and calibrated with a Theropithecus-Papio split of 5 mya based on new fossil evidence (Jablonski et al.,2008; Frost et al., 2014). The main research questions are: (i) AreArabian hamadryas baboons genetically distinct from Africanhamadryas baboons? (ii) Do Arabian baboons exhibit populationsubstructure? (iii) When, and via which route, did baboons colo-nize Arabia?

Materials and methods

Sample collection

We non-invasively obtained baboon faecal samples at 37 sites inEritrea, Ethiopia, and Yemen, identified species based on pheno-typic characters, and recorded the GPS coordinates of each samplingsite (Fig. 2, Table 1). Fresh samples were preserved in 90% ethanol.Dry samples were preserved in plastic tubes without an additive.Sampleswere stored at ambient temperature for up to sixmonths inthe field and at �20 �C upon arrival in the laboratory. Additionally,tissue samples of Arabian hamadryas baboonswere provided by theKing Khalid Wildlife Research Centre (KKWRC), Saudi Arabia. Eartissue was taken from anaesthetized animals, which were live-trapped and released during a population genetic survey (Winneyet al., 2004; Hammond et al., 2006). We also included mtDNAsequence information from one yellow baboon museum specimenfrom Somalia (Zinner et al., 2008). Sample collection, as well ascapturing and handling procedures of baboons, complied with thelaws of the respective countries of origin and Germany and theguidelines from the International Primatological Society.

DNA extraction, PCR amplification, and sequencing

DNA from tissue and faeceswas extracted using theDNeasy BloodandTissueKit (Qiagen,Hilden,Germany) andQiAampDNAStoolMiniKit (Qiagen), respectively. Extraction was according to the manufac-turer's protocols with slight modifications (Haus et al., 2013). Toprevent contamination, laboratory procedures followed standardprotocols (Goossens et al., 2000; Karanth et al., 2005; Osterholz et al.,2008; Roos et al., 2008). DNA extraction, PCR, gel extraction, andsequencingwereperformedinseparate laboratories.All PCRreactionswere performed with negative (HPLC-purified water) controls.

We analysed three mitochondrial markers, as these allowed usto include published data sets in the statistical analyses and theycould reliably be amplified from low quality samples. Furthermore,since mtDNA is transmitted via the maternal lineage, and becausein hamadryas baboons females are the predominant dispersing sex,these markers are expected to give a good indication of the popu-lation history of this species. We amplified and sequenced a 338 bpfragment of the mitochondrial HVRI (Hapke et al., 2001) of allsamples. For a subset, representing all major mitochondrial cladesdiscovered in the HVRI analysis, we also sequenced 896 bp of theBrown Region and 1140 bp of the cytochrome b gene (cyt b) usingestablished protocols (Zinner et al., 2009). Brown Region and cyt bwere both amplified via two overlapping fragments to ensure thatsequences were obtained even if the DNA was degraded (as can beexpected in faecal samples). To prevent amplification of nuclearpseudogenes, we used primers known to solely amplify the mito-chondrial fragment (Zinner et al., 2009). The PCR conditions foramplifications comprised a pre-denaturation step at 94 �C for2 min, followed by 40 cycles at 94 �C for 1 min, 51 �C (HVRI)/56 �C(Brown Region)/60 �C (cyt b) for 1 min and 72 �C for 1 min, and afinal extension step at 72 �C for 5 min. The results of the PCR am-plifications were checked on 1% agarose gels. The PCR productswere cleaned with the Qiagen PCR Purification Kit and

Figure 2. Baboon sampling sites (see also Table 1) in Africa and Arabia. Dashed lines indicate approximate geographic range of hamadryas baboons in Africa and Arabia.

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164 157

subsequently sequenced on an ABI 3130xL sequencer using theBigDye Terminator Cycle Sequencing Kit (Applied Biosystems).

Analyses

Sequences were checked, edited and aligned manually usingBioEdit 7.5.0.2 (Hall, 1999). The data set was complemented withpublished orthologous sequences from Eritrea and Saudi Arabiaavailable in GenBank [AF275384-AF275475 (Hapke et al., 2001);AY247444-AY247447, AY247453, AY247459, AY247460, AY247530,AY247533, AY247534, AY247547, AY247548 (Winney et al., 2004)].The resulting final data set comprised 294 HVRI sequences from 43localities (10 Arabia and 33 Africa, including eight P. anubis sites andthree P. anubis � P. hamadryas hybrid sites in Eritrea and Ethiopia).For divergence time estimates we used 73 concatenated BrownRegion þ cyt b þ HVRI sequences from 28 sites (nine Arabia and 19Africa, including seven P. anubis sites in Eritrea and Ethiopia, andone P. anubis � P. hamadryas hybrid site in Ethiopia) comprising 52haplotypes. As outgroups, we used orthologous sequences fromTheropithecus gelada and 17 Papio spp. samples from other regions

in Africa, including 15 P. anubis samples from southern Ethiopia andone P. cynocephalus sample from south-eastern Somalia. The finalalignment comprised 70 sequences (52 þ 18). All sequences weredeposited in GenBank (details of samples, amplified loci per sample,and accession numbers are given in Appendix A, SupplementaryOnline Material [SOM] Table S1).

We used the HVRI data set to investigate the genetic populationstructure of hamadryas baboons in detail. To visualize the rela-tionship between haplotypes, we reconstructed a median-joininghaplotype network (Bandelt et al., 1999) using Network version4.6.1.1 (2012 Fluxus Technology Ltd.). Here we left out the 15Ethiopian olive baboons, as they are too distantly related. Hence,only 280 samples were included in the network analysis.

To compare genetic diversity for hamadryas baboons in Africaand Arabia, we calculated haplotype diversity (Hd) and nucleotidediversity (p) using DnaSP 5.10.1 (Librado and Rozas, 2009), andtested the differences for significance using Statistica 10 (StatSoft®).Additionally, we investigated the distribution of genetic diversity inthe Arabian population by calculating Hd and p for each samplinglocality (excluding localities with only one sample).

Table 1Geographic coordinates (decimal degrees) of Papio sampling sites and sample sizes.

No. Taxon Country Site Code Samplesize

Longitude Latitude

1 Ph Saudi Arabia Abha Abh 25 42.505228 18.2163892 Ph Saudi Arabia Al Akhal Akl 6 39.859444 23.3155563 Ph Saudi Arabia Baha Bah 15 41.466667 20.0166674 Ph Saudi Arabia Dhilafa Escp. Dhi 4 42.466667 17.9333335 Ph Saudi Arabia Taif Tif 15 40.415833 21.2702786 Ph Yemen Bura'a Forest A BuH 4 43.416667 14.8666677 Ph Yemen Bura'a Forest B BuL 5 43.866944 14.8672228 Ph Yemen Jebel Iraf Ira 1 44.250000 13.1166679 Ph Yemen Jebel Raymah Ray 1 43.433333 14.66666710 Ph Yemen Jebel Sabir Sab 1 44.200000 13.58333311 Ph Eritrea Mt. Abagamsei Aba 14 39.018620 15.34910012 Ph Eritrea Abdur Abd 11 39.845850 15.12857013 Ph Eritrea Afabet Afb 3 38.749583 16.12016614 Ph Eritrea Barka Bridge Bbr 7 38.020380 15.55512015 Ph Eritrea R. Baeat Bea 2 38.094270 15.67157016 Ph Eritrea Dada (Bolo) Dad 13 42.508889 13.12963017 Ph Eritrea Debresina Deb 3 38.825930 15.70535018 Ph Eritrea Dogali Dog 6 39.284730 15.57908019 Ph Eritrea Durfo Dur 7 38.964580 15.37370020 Ph Eritrea Filfil Bridge Fil 6 38.944450 15.61442021 Ph Eritrea Furrus Fur 9 38.971150 15.01148022 Ph Eritrea Geleb Gel 7 38.824070 15.82143023 Ph Eritrea Halhal Hal 7 38.314330 15.94137024 Ph Eritrea Af Himbol Him 9 37.397100 15.94505025 Ph Eritrea Kubkub Kub 11 38.632170 16.34482026 Ph Eritrea Mensura Men 5 38.351230 15.44598027 Ph Eritrea Molki Mol 7 38.221700 14.90908028 PX Eritrea R. Shackat Sha 4 37.499350 14.98310029 Pa Eritrea R. Griset Gri 8 36.760180 14.88322030 Pa Eritrea R. Hadejemi Had 6 36.907100 14.35827031 Pa Eritrea Haykota Hay 17 37.066000 15.15695032 Pa Eritrea Tesseney Tes 9 36.701420 15.14510033 Ph Ethiopia Awash Station ASt 5 40.177750 8.99268334 Ph Ethiopia Gerba Luku Ger 10 41.534000 9.58740035 Ph Ethiopia Mieso Mie 7 40.764083 9.20353336 PX Ethiopia Awash Falls AFa 5 40.019167 8.84268337 PX Ethiopia Wolenkiti Wol 5 39.487883 8.69458338 Pa Ethiopia Adami Tulu Ada 4 38.714933 7.82558339 Pa Ethiopia Alambada Ala 3 38.747683 7.50463340 Pa Ethiopia Managasha 1 Mng 1 38.583333 9.08333341 Pa Ethiopia Managasha 2 Man 6 38.571250 8.96838342 Pa Ethiopia Wendo Genet Wen 1 38.649650 7.07126743 Pc Somalia Webi Shebelli Web 1 45.433333 2.420833

Ph ¼ Papio hamadryas; Pa ¼ P. anubis; PX ¼ phenotypic hybrids betweenP. hamadryas and P. anubis; Pc ¼ P. cynocephalus. Longitude and latitude in decimaldegrees.

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164158

To investigate whether the Arabian baboon populationexpanded after the colonization event, we calculated mismatchdistributions for both Arabian clades in Arlequin 3.5.1.3 (Excoffierand Lischer, 2010) with 1000 bootstraps. We tested both themodel for demographic expansion and the model for spatialexpansion. We then calculated the time since expansion witht ¼ 2mt (m: mutation rate, t: number of generations since expan-sion). Here we applied a generation time of 12 years (Rogers andKidd, 1996) and the specific mutation rate of primate HVRI of15e20% per million years (Jensen-Seaman and Kidd, 2001).

To estimate divergence times between clades, we concatenatedthe Brown Region, cyt b, and HVRI sequences (n¼ 70), and applied aBayesian Markov Chain Monte Carlo method, which employs arelaxed molecular clock approach (Drummond et al., 2006) asimplemented in BEAST 1.6.1 (Drummond and Rambaut, 2007). Thethree loci were partitioned, each with its optimal nucleotide sub-stitution model (Brown Region: TrN þ G; cyt b: HKY þ G; HVRI:HKY þ I þ G) as chosen with the Bayesian information criterion(BIC) in jModeltest 0.1.1 (Posada, 2008). We assumed a relaxeduncorrelated lognormal model of lineage variation and a Birth-Death Process prior for branching rates. As a calibration point,

we applied the fossil-based split of Theropithecus and Papio 5.0 ± 1.0mya (Jablonski et al., 2008; Frost et al., 2014). Four replicates wererun for 25 million generations with tree and parameter samplingoccurring every 100 generations. The adequacy of a 10% burn-in andconvergence of all parameters was assessed by visual inspectionof the trace of the parameters across generations using TRACER1.5 (Rambaut et al., 2003). The sampling distributions were com-bined (25% burn-in) using LogCombiner 1.6.1 (Rambaut andDrummond, 2002a). A consensus chronogram with node heightdistributionwas generated and visualized with TreeAnnotator 1.6.1(Rambaut and Drummond, 2002b) and FigTree 1.3.1 (Rambaut,2006).

Results

The 294 baboon samples comprised 109 HVRI haplotypes. Thesubset of 73 samples for which we analysed the Brown Region, cytb, and HVRI, comprised 52 haplotypes.

Haplotype network

The HVRI haplotype network reveals three major clades (Fig. 3).Clade X is strictly African and consists of Eritrean and a few Ethio-pian hamadryas baboons, and phenotypical P. hamadryas� P. anubishybrids from Ethiopia. Clade Y is more complex, encompassingEritrean hamadryas and olive baboons, Eritrean hybrids, andArabian hamadryas baboons. Clade Z comprises Ethiopian, Eritrean,and Arabian hamadryas baboons. Two Arabian clades are identifi-able. Clade Arab_Y comprises four haplotypes and clusters closelywith Eritrean baboons. Clade Arab_Z consists mainly of haplotypesfound in Arabia but also some haplotypes found in Eritrea fromsampling locations closest to the Bab-el-Mandab Strait (Dad) andone haplotype from Gerba Luku, Ethiopia (0317PHGer). CladeArab_Z clusters more closely with Ethiopian baboons.

Population genetics of Arabian baboons

Whereas the three northern Arabia sampling locations (Akla,Taif, and Baha) harbour only haplotypes of Clade Arab_Z, bothClades Arab_Z and Arab_Y are represented in all other locations inArabia (Fig. 4). One haplotype (H1) of Clade Arab_Z is found in everysampling location in Arabia.

Haplotype diversity and nucleotide diversity are both signifi-cantly higher in the African than in the Arabian hamadryas baboonpopulations (nAfrica ¼ 149, nArabia ¼ 77, HdAfrica ± SD ¼ 0.983± 0.003, HdArabia ± SD ¼ 0.871 ± 0.026, p < 0.001; pAfrica ± SD¼ 0.04251 ± 0.00088, pArabia ± SD ¼ 0.01920 ± 0.00243, p < 0.001).Haplotype diversity and nucleotide diversity are both significantlyhigher (p < 0.001) in Clade Arab_Z (n ¼ 61) than in Clade Arab_Y(n¼ 16): (HdZ ± SD¼ 0.825 ± 0.040, HdY ± SD¼ 0.533 ± 0.142) andpZ ± SD ¼ 0.00431 ± S0.00046, pY ± SD ¼ 0.00218 ± 0.00076.

When genetic diversity for Arabian hamadryas baboons isdepicted from south to north, a decrease is observed in nucleotidediversity but not in haplotype diversity (Fig. 5). Both Arabian cladesprobably underwent a population expansion, as neither the de-mographic nor the spatial expansion model is rejected at a ¼ 5%(Table 2). The expansion of Clade Arab_Z occurred twice as early asthe expansion of Clade Arab_Y, as indicated by a t value, which istwice as high (Table 2).

Phylogenetic tree and divergence time estimates

Similar to the network, the phylogenetic tree reconstruction,based on concatenated Brown þ cyt b þ HVRI sequences, revealsthe three distinct Clades X, Y, and Z, all of which include African

Figure 3. Median-joining HVRI haplotype network of hamadryas baboons with the three major clades X, Y, and Z indicated by grey shading and the two Arabian clades Arab_Y andArab_Z indicated by dashed boxes (n ¼ 280, 338 bp). Scale bar ¼ 1 pairwise difference; node sizes are proportional to haplotype frequencies (scale indicates 1, 5, 10 and 20). (Forinterpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164 159

hamadryas baboons (Fig. 6). Clade X is purely African and includesboth hamadryas and olive baboons. Clade Y is more complex,encompassing Eritrean hamadryas and olive baboons, as well asArabian hamadryas baboons. Clade Z comprises Ethiopian, coastal

Figure 4. HVRI haplotypes network of Arabian hamadryas baboons showing thespatial distribution and frequency of haplotypes.

Eritrean, and Arabian hamadryas baboons. African hamadryas ba-boons in Clades Y and Z are basal to Arabian hamadryas baboons,pointing to an African origin for this species.

In Clade Z, Arabian and coastal Eritrean baboons are estimatedto have diverged from the Ethiopian population 150.4 kya (95%confidence interval: 221.8e87.5). Arabian lineages diverged fromcoastal Eritrean baboons 77.2 (119.1e41.4) kya. The first split withinClade Arab_Z is estimated at 54.7 (84.7e28.2) kya and the lineage ofthe Ethiopian sample (0317PHGer) within this clade split off ca.28.0 (47.4e12.4) kya. In Clade Y, Arabian baboons diverged fromEritrean baboons 61.6 (96.4e28.1) kya. The first split within CladeArab_Y is estimated at 30.6 (55.2e10.5) kya (Fig. 6). It can beassumed that baboons immigrated to Arabia between the diver-gence of the African and Arabian lineages and the first splits withinthe Arabian lineages (i.e., between 150 and 31 kya). This timeperiod includes sea level lowstands around 130 kya and 65 kya(Fig. 7). The confidence intervals are, however, large and all diver-gence time estimates span periods of sea level lowstands as well asGreen Sahara Periods (Fig. 7).

Discussion

Our large data set allows us to reconcile and refine previouspopulation genetic studies on hamadryas baboons and therebyelucidate the phylogeographic history of this species. Our resultsindicate that Arabian hamadryas baboons are genetically distinctfrom African hamadryas baboons; they form two mitochondrialclades and share no haplotypes.

African hamadryas baboon populations do not form clearmonophyletic geographic clusters. This is likely attributable tothe female-biased dispersal pattern in this species, which reducesthe correlation between geography and mitochondrial genetic

Figure 5. South-north gradients in Arabian hamadryas baboons in (a) nucleotide diversity and (b) haplotype diversity.

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164160

structuring. This is in support of a recent study that discusses thistopic in detail (Kopp et al., 2014). The inclusion of Ethiopian andEritrean olive baboons in the network is probably due to intro-gression of hamadryas populations by male olive baboons. This haslikely resulted in nuclear swamping and a phenotypical olive ba-boon population carrying hamadryas baboon mitochondria(Wildman et al., 2004; Zinner et al., 2009).

The phylogenetic tree reconstruction and the comparison ofgenetic diversity both support an African origin for hamadryasbaboons. First, the African population is basal in the phylogenetictree, whereas the Arabian clades are derived and nested within theAfrican population. This is in congruence with previous molecularstudies on the origin of hamadryas baboons (Wildman et al., 2004;Winney et al., 2004) and also fits with the fossil record (Alemsegedand Geraads, 2000). Second, one expects the highest genetic di-versity in the region of origin (Austerlitz et al., 1997; Ramachandranet al., 2005; Excoffier et al., 2009), and the African populationharbours a higher mitochondrial genetic diversity than the Arabianpopulation. It cannot be concluded, however, that the immigrationto Arabia imposed a bottleneck effect, as Lawson Handley et al.(2006) found that allelic richness, averaged over seven autosomalloci, is not significantly different between African and Arabianhamadryas baboon populations.

The Arabian baboon population is mitochondrially structuredand composed of two discrete mitochondrial clades. This can beexplained by either two independent colonization events of Arabiaor by a founding population that was already mitochondriallystructured. Two factors support the first alternative. First, the dis-similar geographic distributions of the two clades in Arabia arebetter explained by two colonization events (Wildman, 2000;Wildman et al., 2004; Winney et al., 2004; Fernandes, 2009).Clade Arab_Y, which diverged from the Eritrean hamadryas popu-lation, is restricted to the southern part of the Arabian distribution,while Clade Arab_Z, which diverged from the Ethiopian population,is found in every Arabian sampling location. Second, genetic di-versity is higher in Clade Arab_Z and population expansion andradiation of this clade seem to be slightly less recent than of CladeArab_Y. This makes it more likely that Clade Arab_Z colonizedArabia before Clade Arab_Y, despite the fact that the confidenceintervals of divergence time estimates overlap to a great extent.

Table 2Analysis of mismatch distribution to test for population expansion for both Arabian ham

HVRI clade Demographic expansion Spatial

t (confidence interval) p-value t (confidence inte

Arab_Z 1.566 (1.062e2.271) 0.14 1.565 (0.692e2.0Arab_Y 0.824 (0.000e1.803) 0.999 0.804 (0.227e1.9

Arab_Z and Arab_Y. Calculations are based on a 338 bp fragment of themitochondrial HVRwith t¼ 2mt (m: mutation rate, t: number of generations since expansion; ka¼ thousand yHVRI of 15e20% per million years.

The Clade Arab_Z includes some African samples: one from avery distant location in Ethiopia (Gerba Luku, Ger) and several fromthe sampling site closest to the Bab-el-Mandab Strait on the coast ofEritrea (Dada, Dad). The close relationship between Arabian andcoastal Eritrean baboons indicates natural colonization via the Bab-el-Mandab Strait. Our results cannot resolve whether the coastalEritrean clade is originally African or represents a back-migrationfrom Arabia to Africa. The most likely explanation for the samplefrom Gerba Luku (located on an ancient trade route in the RiftValley) is that humans translocated baboons inland from the coast.Even today, infant and juvenile baboons are kept as pets by nomadsand carried over long distances in Eritrea and Ethiopia (DZ, Per-sonal observation).

We aimed to infer the colonization route of hamadryas baboonsto Arabia through the geographic distribution of genetic diversity,the timingof population expansions, anddivergence time estimates,but the results are ambiguous. There are several alternative sce-narios that could explain the decline in genetic diversity in Arabiafrom south to north. First, this gradient could indicate that hama-dryas baboons colonized Arabia in the south and then expandednorthwards, gradually losing genetic diversity by serial founder ef-fects (Ramachandran et al., 2005; Henn et al., 2012). Second, theobserved pattern could be the result of an initial colonization via thenorthern route by Clade Arab_Z during Green Sahara Periods fol-lowed by a more recent colonization, via the southern route, by in-dividuals belonging to Clade Arab_Y. Third, this pattern is inconcordance with immigration to Arabia via the northern routefollowed by a retraction of the Arabian population to a southernrefugium during dry periods and subsequent northward expansionduring humidperiods. The two latter scenarioswould, however, stillinvolveback-immigrations of CladeArab_Z individuals toAfricavia asouthern route in order to explain the occurrence of closely relatedhaplotype(s) in Africa near the Bab-el-Mandab Strait.

The star-like structure of the Arabian clades and mismatch dis-tributions suggest that, after the colonization of Arabia, both cladesexpanded. The estimated expansion times are both less recent thanthe estimated divergence times and fit with colonization eventsduringMIS 6 (ca.130 kya). These estimates are directly derived fromthe assumed mutation rate. If we assumed a higher mutation rate,because substitution rates are elevated close to the tips (Ho et al.,

adryas baboon lineages.

expansion Time since expansion (ka)

rval) p-value 15% [m ¼ 5.07�10�5] 20% [m ¼ 6.76�10�5]

58) 0.085 185 (82e269) 139 (61e202)58) 0.85 98 (0e232) 73 (0e174)

I and tested for significance with 1000 bootstraps. Time since expansion is calculatedears) applying a generation time of 12 years and the specificmutation rate of primate

Figure 6. Bayesian divergence time estimations of Northeast African and Arabian baboon mtDNA lineages (concatenated Brown region þ cyt b þ HVRI, 2373 bp) based on 52 uniqueNortheast African and Arabian hamadryas baboon haplotypes, 17 other Papio, and one Theropithecus haplotype. In order to conserve space, only the Northeast African and Arabianparts of the tree are depicted. Clades are collapsed and represented as solid triangles. Node values are divergence time estimates in mya, with blue bars across nodes representingtheir 95% highest posterior density intervals. Stars demark nodes with high posterior probabilities (>0.95). (For interpretation of the references to colour in this figure legend, thereader is referred to the web version of this article.)

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164 161

2011), the time estimates of population expansions in Arabia wouldcorrespond better with the divergence times estimates.

Combining divergence time estimates with climatic data couldhelp to identify the most probable of the above-mentioned sce-narios. One has to bear in mind, however, that proposed periods ofsea level lowstands and the existence of a land bridge across thesouthern Red Sea are still highly debated (Fernandes et al., 2006;Bailey, 2009), that climatic reconstructions are far from precise(Drake et al., 2013), and that the confidence intervals of ourdivergence time estimates span large intervals. Therefore, it is vitalto stress the limitations of the data. In concordance with previousstudies (Wildman, 2000; Wildman et al., 2004; Winney et al.,

Figure 7. Divergence ages between African and Arabian hamadryas baboon mtDNA clades2009) and Green Sahara Periods (green; Blome et al., 2012; Drake et al., 2013). Numbers 1white-tailed mongoose Ichneumia albicauda (Fernandes, 2011); (2) cheetah Acinonyx jubatuleopard Panthera pardus (Uphyrkina et al., 2001). (For interpretation of the references to co

2004), our divergence times are not recent enough to support anoriginal introduction of hamadryas baboons to Arabia by humans(which would have occurred within the last 10 kya). Our estimates,however, locate the divergence between African and Arabian ba-boons as 222e28 kya. This is more recent than previously thoughtand within the same time frame proposed for the out-of-Africamigration of modern humans, the Late Pleistocene.

The entire time span from the divergence of the Arabian pop-ulation from the African population to the onset of diversificationwithin the Arabian clades needs to be considered as the criticalperiod for the colonization. Our divergence time estimates do nothave the power to resolvewhether the two Arabian clades diverged

in relation to Red Sea sea level lowstands (yellow; Rohling, 1994; Rohling et al., 1998,to 4 refer to estimated colonization times of other African mammals into Arabia: (1)s (Charruau et al., 2011); (3) striped hyena Hyaena hyaena (Rohland et al., 2005); (4)lour in this figure legend, the reader is referred to the web version of this article.)

G.H. Kopp et al. / Journal of Human Evolution 76 (2014) 154e164162

from the African source population at different times. This isbecause of the inclusion of African samples in Clade Arab_Z, lowsupport values within Clade Y, and a great overlap of confidenceintervals. If coastal Eritrean baboons in Clade Z represent a back-immigration to Africa, the colonization of Arabia in this cladebroadly coincides with the proposed period of the sea level low-stand in MIS 6 (ca. 130 kya). The alternative scenario for Clade Z andthe divergence time estimates for Clade Y are both in concordancewith colonization events during MIS 4 (ca. 65 kya; Rohling, 1994;Rohling et al., 1998, 2009) (Fig. 7). Colonizing events during MIS 2(ca. 20 kya) cannot be rejected as the first splits within the ArabianClade Arab_Y (i.e., the onset of diversification within this clade)occurred during this period.

Studies of other terrestrial Afro-Arabian mammals, such aswhite-tailed mongoose Ichneumia albicauda (Fernandes, 2011),cheetah Acinonyx jubatus (Charruau et al., 2011), striped hyenaHyaena hyaena (Rohland et al., 2005), and leopard Panthera pardus(Uphyrkina et al., 2001) do not reveal any congruent pattern (Fig. 7).For humans, MIS 5 (ca. 130e71 kya) is identified as the climaticperiod most probable for dispersal for both immigration routes(Drake et al., 2013). Immigrations by hamadryas baboons throughthe northern route were probably feasible during major GreenSahara Periods (Blome et al., 2012; Drake et al., 2013; Larrasoa~naet al., 2013), which fall well within the divergence confidence in-tervals of both Arabian clades. Hamadryas baboons historically(3000e2000 B.C.E.) occurred farther north to Upper Egypt and olivebaboons penetrated the Sahara (Smith, 1969; Arnold, 1995 cited in;Masseti and Bruner, 2009). There is, however, to our knowledge, noarchaeological evidence for baboons on the Sinai Peninsula, theLevant or northern Arabia to support a historic occurrence alongthe northern route. It is also important to note that dispersal via thesouthern route might have occurred by means other than landbridges (Bailey et al., 2007), e.g., over-water dispersal, as has beenproposed in a variety of contexts for other mammals, includingprimates (Yoder et al., 2003; de Queiroz, 2005; Fernandes et al.,2006; Fernandes, 2011).

Independent of the route the baboons took, an interestingquestion remains, ‘Why did hamadryas baboons not emigratefarther east into Oman?’, especially because humans are proposedto have emigrated eastward through southern Arabia between 70kya and 50 kya (Kivisild et al., 1999; Oppenheimer, 2012a,b).Favourable humid conditions in southern Arabia likely occurredaround 125.0 kya, 100.0 kya and 80.0 kya, whereas from 75.0 kya to10.5 kya arid conditions prevailed and turned southern Arabia intoa natural barrier for baboon dispersal (Yan and Petit-Maire, 1994;Groucutt and Petraglia, 2012; Rosenberg et al., 2012).

Our results favour the southern route hypothesis over thenorthern route hypothesis, and also indicate a more recent andcomplex colonization of Arabia than previously thought (Wildmanet al., 2004; Winney et al., 2004; Fernandes, 2009). The closerelationship between the Arabian population and the Africanpopulation nearest to the Bab-el-Mandab Strait supports the hy-pothesis that this region served as an important dispersal corridorbetween Africa and Arabia (Wildman, 2000; Kivisild et al., 2004).We conclude that (i) the present distribution and diversity ofhamadryas baboons is shaped by a colonization of Arabia fromAfrica via a southern route in the Late Pleistocene and by back-immigrations to Africa, and (ii) that humans did not play a role inthe original colonization of Arabia by hamadryas baboons.

Acknowledgements

We thank Dawit Berhane for helping to collect samples inEritrea, Karim Nasher for providing samples from Yemen and SaudiArabia, and King Khalid Wildlife Research Centre for providing

samples from Saudi Arabia. Tanja Haus kindly assisted in the lab.We also thank Spartaco Gippoliti and Colin Groves for comments onthe manuscript, Sarah Elton who kindly answered queries aboutPapio fossils, Stephen R. Frost and Christopher C. Gilbert for adviceconcerning the date of the Papio-Theropithecus split, and all mem-bers of the Cognitive Ethology Laboratory for discussions. We aregrateful to Sarah Elton, the Associate Editor of the Journal of HumanEvolution, and two anonymous reviewers whose comments greatlyimproved the final manuscript.

Appendix A. Supplementary online material

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jhevol.2014.08.003.

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